Buccal oscillation and lung ventilation in a semi-aquatic turtle, Platysternon megacephalum

Druzisky, Kelly A.; Brainerd, Elizabeth L.

doi:10.1078/0944-2006-00015

Cited by 22 publications

(21 citation statements)

References 19 publications

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“…The anuran buccal oscillator and/or rhythm have been proposed to be homologous with nonrespiratory rhythms in other amniotes, including sniffing or panting in reptiles (Druzisky and Brainerd, 2001;Brainerd, 1999), and hiccups and/or suckling in man (Straus et al, 2003). These behaviors require careful coordination with the respiratory rhythm (Newsom Davis, 1970;Lau et al, 2003), and therefore the rhythm generators that subserve these functions are likely to be coupled with the respiratory rhythm generator.…”

Section: Other Possible Fates Of the Buccal Oscillatormentioning

confidence: 97%

Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats

et al. 2005

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Though the mechanics of breathing differ fundamentally between amniotes and "lower" vertebrates, homologous rhythm generators may drive air breathing in all lunged vertebrates. In both frogs and rats, two coupled oscillators, one active during the inspiratory (I) phase and the other active during the preinspiratory (PreI) phase, have been hypothesized to generate the respiratory rhythm. We used opioids to uncouple these oscillators. In the intact rat, complete arrest of the external rhythm by opioid-induced suppression of the putative I oscillator, that is, pre-Bötz-inger complex (PBC) oscillator, did not arrest the putative PreI oscillator. In the unanesthetized frog, the comparable PreI oscillator, that is, the putative buccal/ gill oscillator, was refractory to opioids even though the comparable I oscillator, the putative lung oscillator, was arrested. Studies in en bloc brainstem preparations derived from both juvenile frogs and metamorphic tadpoles confirmed these results and suggested that opioids may play a role in the clustering of lung bursts into episodes. As the frog and rat respiratory circuitry produce functionally equivalent motor outputs during lung inflation, these data argue for a close homology between the frog and rat oscillators. We suggest that the respiratory rhythm of all lunged vertebrates is generated by paired coupled oscillators. These may have originated from the gill and lung oscillators of the earliest air breathers.

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Section: Other Possible Fates Of the Buccal Oscillatormentioning

confidence: 97%

Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats

et al. 2005

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“…Previous studies have shown conclusively that gular oscillations do not contribute to lung ventilation in resting turtles (e.g. McCutcheon, 1943;Druzisky and Brainerd, 2001), but none of these studies measured ventilation during locomotion.…”

Section: Lung Ventilation During Turtle Locomotionmentioning

confidence: 99%

“…Small buccal oscillations (<0.4·ml) were recorded during locomotor and non-locomotor behavior, and were distinguished from lung ventilations by expansion and contraction of the throat region (visible in video recordings). Gular pumping for lung ventilation would be evident in airflow traces as small inhalations followed by little or no exhalatory airflow (Owerkowicz et al, 2001;Druzisky and Brainerd, 2001). No such airflow pattern was ever observed in Terrapene carolina, indicating that gular pumping for lung ventilation does not occur in this species (or in any other turtle studied to date; Mitchell and Morehouse, 1863;Hansen, 1941;McCutcheon, 1943;Gans and Hughes, 1967;Gaunt and Gans, 1969;Druzisky and Brainerd, 2001).…”

Section: Morphologymentioning

confidence: 99%

Lung ventilation during treadmill locomotion in a terrestrial turtle,Terrapene carolina

Landberg

Mailhot

Brainerd

2003

Journal of Experimental Biology

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SUMMARYThe limb girdles and lungs of turtles are both located within the bony shell, and therefore limb movements during locomotion could affect breathing performance. A mechanical conflict between locomotion and lung ventilation has been reported in adult green sea turtles, Chelonia mydas, in which breathing stops during terrestrial locomotion and resumes during pauses between bouts of locomotion. We measured lung ventilation during treadmill locomotion using pneumotach masks in three individual Terrapene carolina (mass 304-416 g) and found no consistent mechanical effects of locomotion on breathing performance. Relatively small tidal volumes(2.2±1.4 ml breath-1; mean ± s.d., N=3 individuals) coupled with high breath frequencies(36.6±26.4 breaths min-1; mean ± s.d., N=3 individuals) during locomotion yield mass-specific minute volumes that are higher than any previously reported for turtles (264±64 ml min kg-1; mean ± s.d., N=3 individuals). Minute volume was higher during locomotion than during recovery from exercise(P<0.01; paired t-test), and tidal volumes measured during locomotion were not significantly different from values measured during brief pauses between locomotor bouts or during recovery from exercise(P>0.05; two-way ANOVA). Since locomotion does not appear to conflict with breathing performance, the mechanism of lung ventilation must be either independent of, or coupled to, the stride cycle. The timing of peak airflow from breaths occurring during locomotion does not show any fixed phase relationship with the stride cycle. Additionally, the peak values of inhalatory and exhalatory airflow rates do not differ consistently with respect to the stride cycle. Together, these data indicate that T. carolina is not using respiratory-locomotor coupling and limb and girdle movements do not contribute to lung ventilation during locomotion. X-ray video recordings indicate that lung ventilation is achieved via bilateral activity of the transverse (exhalatory) and oblique (inhalatory) abdominal muscles. This specialized abdominal ventilation mechanism may have originally circumvented a mechanical conflict between breathing and locomotion in the ancestor of turtles and subsequently allowed the ribs to abandon their role in lung ventilation and to fuse to form the shell.

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“…Many instances of buccal oscillation were observed in Tr. scripta at rest, but as has been concluded in every previous study of turtle breathing (contra Agassiz, 1857), these oscillations were ventilating the buccal cavity and not the lungs (Mitchell and Morehouse, 1863;McCutcheon, '43;Druzisky and Brainerd, 2001;Landberg et al, 2003). We conclude that the ventilation mechanism used during locomotion in Tr.…”

Section: Discussionmentioning

confidence: 54%

Lung ventilation during treadmill locomotion in a semi‐aquatic turtle, Trachemys scripta

2008

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It is reasonable to presume that locomotion should have a mechanical effect on breathing in turtles. The turtle shell is rigid, and when the limbs protract and retract, air in the lungs should be displaced. This expectation was met in a previous study of the green sea turtle, Chelonia mydas; breathing completely ceased during terrestrial locomotion (Jackson and Prange, 1979. J Comp Physiol 134:315-319). In contrast, another study found no direct effect of locomotion on ventilation in the terrestrial box turtle, Terrapene carolina (Landberg et al., 2003. J Exp Biol 206:3391-3404). In this study we measured lung ventilation during treadmill locomotion in a semi-aquatic turtle, the red-eared slider, Trachemys scripta. Sliders breathed almost continuously during locomotion and during brief pauses between locomotor bouts. Tidal volume was relatively small (approximately 1 mL) during locomotion and approximately doubled during pauses. Minute ventilation was, however, not significantly smaller during locomotion because breath frequency was higher than that during the pauses. We found no consistent evidence for phase coupling between breathing and locomotion indicating that sliders do not use locomotor movements to drive breathing. We also found no evidence for a buccal-pump mechanism. Sliders, like box turtles, appear to use abdominal musculature to breathe during locomotion. Thus, locomotion affects lung ventilation differently in the three turtle species studied to date: the terrestrial Te. carolina shows no measurable effect of locomotion on ventilation; the semi-aquatic Tr. scripta breathes with smaller tidal volumes during locomotion; and the highly aquatic C. mydas stops breathing completely during terrestrial locomotion.

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Buccal oscillation and lung ventilation in a semi-aquatic turtle, Platysternon megacephalum

Cited by 22 publications

References 19 publications

Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats

Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats

Lung ventilation during treadmill locomotion in a terrestrial turtle,Terrapene carolina

Lung ventilation during treadmill locomotion in a semi‐aquatic turtle, Trachemys scripta

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